Global Ecology and Conservation 3 (2015) 163–175

Contents lists available at ScienceDirect

Global Ecology and Conservation

journal homepage: www.elsevier.com/locate/gecco

Original research article Decapod assemblages in subtidal and intertidal zones—Importance of scuba diving as a survey technique in tropical reefs, Brazil

Bruno Welter Giraldes a,∗, Petrônio Alves Coelho Filho b, David Mark Smyth a a Environmental Studies Center (ESC), Qatar University (QA), Doha, Qatar. P.O. Box 2713, Qatar b Departamento de Engenharia de Pesca, Universidade Federal de Alagoas. Avenida Divaldo Suruagy, s/n, Centro, 57200-000, Penedo, AL, Brazil h i g h l i g h t s

• The significance and importance of scientific diving to study decapods. • Scientific diving allows access to specific decapod assemblages. • The most endangered trade decapods can be targeted on nocturnal dives. • We present an ecological database for subtidal and intertidal decapods. • The first ecological baseline data for decapods in the tropical coastal reefs. article info a b s t r a c t

Article history: Decapods play a crucial role within the reef ecosystem and the development of scuba Received 28 October 2014 diving as a survey tool has allowed researchers the opportunity to study the decapod–reef Received in revised form 23 November relationship more comprehensively. The present study describes the differences in decapod 2014 assemblages in intertidal and subtidal zones at a tropical coastal reef system in the Accepted 23 November 2014 southwestern Atlantic Ocean and reports the importance of scuba diving as a survey Available online 26 November 2014 technique. A total of 71 decapods were recorded during the research; 42 in the intertidal zone mainly formed by small endobenthic and 39 in the subtidal zone primarily Keywords: Endangered large species only 10 were found to frequent both sample zones. The study extends the Ornamental species range of Brachycarpus holthuisi Fausto Filho 1966 in Brazil; and also demonstrates how Aquarium hobbyist scuba diving can be used to complement traditional methodologies and vice versa. The Shore reef zonation research shows the advantages of using scuba diving when studying trade endangered Checklist decapods, as the methodology allows access to cryptic habitats such as reef caves Cryptic habit and underwater cavities which were inaccessible when using traditional techniques. In conclusion scuba diving represents a revolutionary non-destructive survey tool allowing the researcher to directly access a specific decapod assemblage in fragile reef environments and in protected marine areas. © 2014 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).

1. Introduction

Within the habitats termed biogenic reefs, coral reefs in particular present some of the highest biodiversity indices recorded and as a result are one of the most important marine ecosystems in the world (Dubinsky and Stambler, 2011).

∗ Corresponding author. E-mail addresses: [email protected] (B.W. Giraldes), [email protected] (D.M. Smyth). http://dx.doi.org/10.1016/j.gecco.2014.11.011 2351-9894/© 2014 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/3.0/). 164 B.W. Giraldes et al. / Global Ecology and Conservation 3 (2015) 163–175

Fig. 1. Map showing the location of Porto de Galinhas reefs, Pernambuco, along the Northeastern Coast of Brazil, highlighting the natural pools and channels between the reef structures. Source: Adapted from Giraldes (2007, 2012).

In the majority of marine ecosystems, including coral reefs one of the key taxon are the . In particular the decapods, which present high species diversity, are an important component in trophic dynamics and are also an important fishery resource throughout the world (Randall, 1967; Abele, 1974; Melo, 1996, 1999; Coelho et al., 2006, 2007, 2008; De Grave et al., 2009; Dubinsky and Stambler, 2011). Decapod assemblage checklists in areas of hard substrate such as rocky reefs and coral reefs usually occur only in in- tertidal and at the beginning of subtidal zones. Specimens are usually sampled in association with substrate with distinct biotope markers such as algae and corals or rocks and sand (Coelho and Ramos-Porto, 1995; Masunari and Dubiaski-Silva, 1998; Melo and Veloso, 2005; Coelho-Filho, 2006; Almeida et al., 2008). However decapods in shallow subtidal waters are usually sampled with indirect methods such as drags, nets and traps and as a result numerous species elude capture and are not included in decapod checklists for coastal sites. In recent years scientific scuba diving has revolutionized subtidal decapod research. As a result many new discoveries have been made in regards to the influence decapods exert within a subtidal ecosystem and the general ecology and biology within the order (Mantelatto et al., 2004; Bouzon and Freire, 2007; Teschima et al., 2012; Alves et al., 2012; Giraldes et al., 2012a,b; Lang et al., 2013). In order to create a comprehensive list of decapod assemblage for subtidal and intertidal zones in the southwestern Atlantic Ocean and highlight the importance of scientific scuba diving to study decapods, the present study aims to produce a list of species with an associated ecological database for a tropical coastal reef using recognized sampling methodologies in the intertidal zone and scientific scuba diving in the subtidal zone.

2. Material and methods

Samples were collected along the coastal biogenic reef at Porto de Galinhas beach (8°30′07′′–8°30′54′′S e 35°00′08′′–34°59′47′′W) (Fig. 1), one of the most visited coastal reef environments in tropical Northeastern Brazil. The reef formation is a reef bank probably derived from the sandstone bedrock wall that runs parallel to the shoreline. As a result of bio-construction (as coral growing), bio-erosion (endobenthic diggers) and erosion from wave action, a cave and hollowed cavity has been formed the actual feature of the reef structure. Corals and epifaunal have settled on the topside and underside of the overhang and this has led to the formation of a top platform of coral structures. In areas densely aggregated the top platforms of reefs are connected forming interconnected caves below the reef surface (Dominguez et al., 1990; Maida and Ferreira, 1997; Leão et al., 2003; Manso et al., 2003)(Figs. 2 and3). During low tides, the intertidal zone of the reef is exposed and can be categorized as the reef top-shelf, which is clearly visible and is made up of tidal pools, natural permanent pools and channels that cross the reef structures (Fig. 1). The reef topography is populated by epibenthic flora and fauna and associated mobile fauna; macro-algae, zoanthids, calcareous algae, scleractinia corals, calcified hydroids, sponges, sea urchins, bryozoans and ascidians, while inside cave and cavities only a few sessile benthic organisms occur (Dominguez et al., 1990; Maida and Ferreira, 1997; Barradas et al., 2010). This study is a review of data yet to be published in scientific journals, only presented as one monograph which describes sampling methodology in the intertidal zone (Austregésilo-Filho, 1992) and one dissertation and thesis were sampling B.W. Giraldes et al. / Global Ecology and Conservation 3 (2015) 163–175 165

Fig. 2. Schematic profile of the reef edge of Porto de Galinhas reefs, highlighting: the intertidal zone, the tidal pools and the exposed reef; and the subtidal zone with the light influenced reef, the cavernous environments with the imaginary line of the shallow zone and the soft bottom surrounding the reefs. Source: Adapted from Giraldes (2007, 2012).

Fig. 3. Schematic profile of one sample point on the reef edge (border) at Porto de Galinhas, highlighting: the intertidal and subtidal zones, the diver and the benthic features such as tidal pools, exposed reef, cave with shadow zone and the sandy soft bottom. Source: Adapted from Giraldes (2007, 2012). was carried out using scientific scuba diving and visual sampling methodology in the subtidal zone (Giraldes, 2007, 2012). Dr. Petrônio Alves Coelho from the crustacean laboratory at Federal University of Pernambuco (UFPE) guided both researches and inspired this checklist study. Specimen voucher samples were deposited in oceanographic museum of the Federal University of Pernambuco (MOUFPE) and/or identified in the laboratory using taxonomic references. Intertidal sampling involved walking along the reef topside during low tide. Animals were collected on exposed reefs, in tide-pools and along the reef fringe until the subtidal zone lineation was met. All species were collected and identified in the laboratory due to the small size of individuals. 166 B.W. Giraldes et al. / Global Ecology and Conservation 3 (2015) 163–175

Fig. 4. Number of species inside each decapod Infraorder (Brachyura, Anomura, Achelata, Gebiidae, Astacidea, and Stenopodidea) and Suborder (), in relation to Subtidal and Intertidal zones in Porto de Galinhas reef.

The subtidal zone was also sampled during a low tide and scuba diving was used at night to collect samples, when decapods are most. All decapods collected were identified in an improvised laboratory close to the survey reef. Large well- known decapods such as large , and ornamental were visually identified in-situ and recorded on an underwater slate. To identify the abundance and frequency of species 12 sample events were carried out at each zone, comprising of 12 subtidal and 12 intertidal samples. Families are presented in evolutionary order and the species in alphabetical order following De Grave et al.(2009) clas- sification. Data was analyzed using: Abundance (Ab)—individual average amounts per sample (Ab = n/s) where n is the number of individuals observed and s is the number of samples held; and the frequency (Fr)—calculated by the formula: Fr = p·100/P, where p is the sample number where the species occurred and P is the total sample number analyzed as following: Constant (75%–100%); Very Common (50%–75%); Common (25%–50%); Occasional (10% ≤ 25%) and Rare (0%–10%) (Based on Dajoz, 2005; Odum and Barrett, 2007).

3. Results

A total of 71 decapods were recorded between subtidal and intertidal zones. Only 10 species were recorded frequenting both sample zones, 1 Anomura and 9 Brachyura (Table 1). Forty-two decapods were recorded along the intertidal zone (Table 1), comprising of 1 Dendrobranchiata, 1 Stenopodidea, 12 Caridea, 1 Gebiidae, 6 Anomura and 21 Brachyura (Fig. 4)(Table 1). The samples mainly contained small decapod species with several endobenthic species. Thirty-nine decapods were recorded subtidally using scuba diving (Table 1), comprising of 1 Dendrobranchiata, 1 Stenopodidea, 4 Caridea, 1 Astacidea, 5 Achelata, 6 Anomura and 21 Brachyura (Fig. 4)(Table 1). They were mainly composed of epibenthic species with large and medium sized animals, almost all with economic value. Abundance analysis of intertidal samples recorded 5 dominant decapods that contributed 56% of the total species abundance. The most prolific species was Palaemon northropi with 21% (25.92 ± 28.13), followed by Microphrys bicornutus 15%(17.58 ± 11.54), Clibanarius antillensis 8% (10.17 ± 9.25) and Mithraculus forceps (7.83 ± 7.14) and Alpheus cf. armillatus (7.33 ± 0.28) each with 6%; the remaining 38 species contributed to 44% of the total abundance (Fig. 5)(Table 1). Abundance within the subtidal samples recorded 5 dominant species with 92%. Being rigens with 53% (27.92 ± 27.43), echinatus 18%(9.59 ± 9.19), Mithraculus forceps 18%(9.38 ± 17.13), Janicea antiguensis 2%(0.81 ± 1.48) and Stenopus hispidus 1%(0.51 ± 1.01); the remaining 34 species represented 8% of the abundance (Fig. 5) (Table 1). In intertidal samples record 12 decapod species were recorded constantly (Palaemon northropi, Cuapetes americanus, Alpheus cf. armillatus, Synalpheus fritzmuellerie, Petrolisthes galathinus, Clibanarius antillensis, Eriphia gonagra, Microphrys bicornutus, Mithraculus forceps, Eurypanopeus abbreviatus, Panopeus hartii and Pachygrapsus transversus), 5 very common, B.W. Giraldes et al. / Global Ecology and Conservation 3 (2015) 163–175 167

Table 1 Decapod assemblage at Porto de Galinhas reefs, Northeastern Brazil. Lines present the species. Columns are of species sampled in Subtidal zone (gray) and Intertidal zone (colorless), with its corresponding values of: Abundance (Ab.) with individuals average and standard deviation; and Frequency (Fr.), being constant (CT), Very Common (VC), Common (Co), Occasional (Oc) and Rare (Rr). ∗ Indicates species absence. Decapod checklist Subtidal Intertidal Ab. Fr. Ab. Fr.

DENDROBRANCHIATA Penaeidae Farfantepenaeus subtilis (Pérez-Farfante, 1967) 0.13 ± 0.38 Oc ∗ ∗ Sicyoniidae Sicyonia parri (Burkenroad, 1934) ∗ ∗ 0.08 ± 0.28 Rr

PLEOCYEMATA STENOPODIDEA Spongicolidae Microprosthema semilaeve (Von Martens, 1872) ∗ ∗ 0.08 ± 0.28 Rr Stenopodidae Stenopus hispidus (Olivier, 1811) 0.51 ± 1.01 Co ∗ ∗

CARIDEA (Gordon, 1936) 27.92 ± 27.43 CT ∗ ∗ Brachycarpus biunguiculatus (Lucas, 1849) 0.09 ± 0.33 Rr ∗ ∗ Brachycarpus holthuisi Fausto Filho, 1966 0.06 ± 0.27 Rr ∗ ∗ Palaemon (Palaeander) northropi Rankin, 1898 ∗ ∗ 25.92 ± 28.13 CT Cuapetes americanus (Kingsley, 1878) ∗ ∗ 6.37 ± 4.86 CT Alpheidae Alpheus cf. armillatus H. Milne Edwards, 1837 ∗ ∗ 7.33 ± 0.28 CT Alpheus cf. formosus Gibbes, 1850 ∗ ∗ 2.83 ± 2.75 VC Alpheus nuttingi (Schmitt, 1924) ∗ ∗ 0.5 ± 1.0 Synalpheus fritzmuelleri Coutière, 1909 ∗ ∗ 3.42 ± 2.19 CT Synalpheus longicarpus (Herrick, 1891) ∗ ∗ 0.08 ± 0.28 Rr Barbouriidae Janicea antiguensis (Chace, 1972) 0.81 ± 1.48 Co ∗ ∗ Hippolytidae Hippolyte obliquimanus Dana, 1852 ∗ ∗ 1.25 ± 2.34 Co Latreutes parvulus (Stimpson, 1866) ∗ ∗ 0.17 ± 0.58 Rr Lysmata rathbunae Chace, 1970 ∗ ∗ 1.5 ± 1.98 Co Thor manningi Chace, 1972 ∗ ∗ 0.58 ± 0.79 Co Processidae Processa fimbriata (Manning e Chace, 1971) ∗ ∗ 0.08 ± 0.28 Rr

ASTACIDEA Enoplometopidae Enoplometopus antillensis (Lütken, 1865) 0.05 ± 0.22 Rr ∗ ∗

GEBIIDEA Upogebiidae Upogebia affinis (Say, 1818) ∗ ∗ 1.67 ± 1.67 VC

ACHELATA Palinuridae Palinurellus gundlachi von Martens, 1878 0.17 ± 0.44 Oc ∗ ∗ (Latreille, 1804) 0.16 ± 0.64 Rr ∗ ∗ (continued on next page) 168 B.W. Giraldes et al. / Global Ecology and Conservation 3 (2015) 163–175

Table 1 (continued)

Decapod checklist Subtidal Intertidal Ab. Fr. Ab. Fr.

Panulirus echinatus Smith, 1869 9.59 ± 9.19 CT ∗ ∗ Panulirus laevicauda (Latreille, 1817) 0.02 ± 0.15 Rr ∗ ∗ Scyllaridae Parribacus antarcticus (Lund, 1793) 0.19 ± 0.44 Oc ∗ ∗

ANOMURA Porcellanidae Megalobrachium mortenseni Haig, 1962 ∗ ∗ 0.08 ± 0.28 Rr Petrolisthes galathinus (Bosc, 1802) ∗ ∗ 4.25 ± 3.93 CT Petrolisthes rosariensis Werding, 1978 ∗ ∗ 0.58 ± 2.02 Rr Diogenidae Calcinus tibicen (Herbst, 1791) 0.24 ± 0.78 Oc 1.42 ± 1.16 Oc Cancellus ornatus Benedict, 1901 0.07 ± 0.46 Rr ∗ ∗ Clibanarius antillensis Stimpson, 1859 ∗ ∗ 10.17 ± 9.25 CT Clibanarius sclopetarius (Herbst, 1796) ∗ ∗ 1 ± 0.85 VC Dardanus venosus (H. Milne Edwards, 1848) 0.01 ± 0.11 Rr ∗ ∗ Paguristes erythrops Holthuis, 1959 0.07 ± 0.26 Rr ∗ ∗ Petrochirus diogenes (Linnaeus, 1758) 0.01 ± 0.08 Rr ∗ ∗ Paguridae Pagurus provenzanoi Forest e de Saint Laurent, 1968 0.43 ± 1.33 Oc ∗ ∗

BRACHYURA Dromiidae Dromia erythropus (Edwards, 1771) 0.01 ± 0.07 Rr ∗ ∗

Calappidae Calappa ocellata Holthuis, 1958 0.02 ± 0.13 Rr ∗ ∗ Calappa sulcata Rathbun, 1898 ∗ ∗ 0.08 ± 0.28 Rr Carpiliidae Carpilius corallinus (Herbst, 1783) 0.01 ± 0.07 Rr ∗ ∗ Eriphiidae Eriphia gonagra (Fabricius, 1781) ∗ ∗ 1.83 ± 1.4 CT Menippidae Menippe nodifrons Stimpson, 1859 0.19 ± 0.49 Oc 0.08 ± 0.28 Rr Leucosiidae Lithadia conica (Coelho, 1973) 0.01 ± 0.07 Rr ∗ ∗

Epialtidae Acanthonyx dissimulatus Coelho, 1993 0.01 ± 0.07 Rr 0.34 ± 0.65 Oc Epialtus bituberculatus (H. Milne Edwards, 1834) ∗ ∗ 0.75 ± 2.01 Oc Pelia rotunda A. Milne Edwards, 1875 0.03 ± 0.2 Rr ∗ ∗ Pitho lherminieri (Desbonne, in Desbonne e Schramm, 0.01 ± 0.11 Rr 0.58 ± 1.16 Oc 1867) Inachidae Stenorhynchus seticornis (Herbst, 1788) 0.21 ± 0.77 Rr ∗ ∗

Majidae Macrocoeloma laevigatum (Stimpson, 1871) ∗ ∗ 0.08 ± 0.28 Rr Microphrys bicornutus (Latreille, 1825) 0.53 ± 1.59 Oc 17.58 ± 11.54 CT Mithraculus forceps A. Milne-Edwards, 1875 9.38 ± 17.13 VC 7.83 ± 7.14 CT Mithrax braziliensis Rathbun, 1892 0.4 ± 0.85 Co 0.42 ± 0.67 Co Mithrax hemphilli Rathbun, 1892 0.19 ± 0.61 Oc 0.34 ± 0.65 Oc Mithrax hispidus (Herbst, 1790) 0.32 ± 0.92 Oc ∗ ∗ (continued on next page) B.W. Giraldes et al. / Global Ecology and Conservation 3 (2015) 163–175 169

Table 1 (continued)

Decapod checklist Subtidal Intertidal Ab. Fr. Ab. Fr.

Nemausa acuticornis (Stimpson, 1870) 0.01 ± 0.07 Rr ∗ ∗ Thoe aspera Rathbun, 1901 ∗ ∗ 0.08 ± 0.28 Rr

Pilumnidae Pilumnus dasypodus Kingsley, 1879 ∗ ∗ 0.5 ± 1.44 Oc

Portunidae Callinectes marginatus (A. Milne-Edwards, 1861) 0.02 ± 0.13 Rr 1.08 ± 1.44 Co Charybdis hellerii (A. Milne Edwards, 1867) 0.02 ± 0.13 Rr ∗ ∗

Domeciidae Domecia acanthophora(Desbonne, in Desbonne e 0.22 ± 0.87 Rr ∗ ∗ Schramm, 1867) Panopeidae Acantholobulus schmitti (Rathbun, 1930) ∗ ∗ 3.75 ± 3.14 VC Hexapanopeus angustifrons (Benedict e Rathbun, 1891) ∗ ∗ 1.67 ± 3.71 Oc Eurypanopeus abbreviatus (Stimpson, 1860) ∗ ∗ 5.85 ± 3.84 CT Panopeus hartii Smith, 1869 ∗ ∗ 3.67 ± 4.77 CT Panopeus occidentalis Saussure, 1857 ∗ ∗ 0.92 ± 2.15 Oc

Xanthidae Cataleptodius floridanus (Gibbes, 1850) ∗ ∗ 1.83 ± 3.61 VC Platypodiella spectabilis (Herbst, 1794) 0.01 ± 0.07 Rr ∗ ∗

Grapsidae Pachygrapsus transversus (Gibbes, 1850) 0.01 ± 0.07 Rr 3.75 ± 3.41 CT Plagusia depressa (Fabricius, 1775) 0.01 ± 0.07 Rr ∗ ∗

(Alpheus formosus, Upogebia affinis, Clibanarius sclopetarius, Acantholobulus schmitti and Cataleptodius floridanus), and 5 com- mon (Hippolyte obliquimanus, Lysmata rathbunae and Thor manningi, Mithrax braziliensis and Callinectes marginatus). Apart from the above species, 9 were occasional and 12 were considered rare (Table 1). Frequency in subtidal samples resulted in only 2 constant decapods (Cinetorhynchus rigens and Smith, 1869), 1 very common (Mithraculus forceps), and 3 common (Janicea antiguensis, Stenopus hispidus and Mithrax braziliensis); 10 species were occasional with largest amount 23 considered rare (Table 1).

4. Discussion

A direct comparison cannot be made between the intertidal samples collected at Austregésilo-Filho, in 1992 and the subtidal samples from Giraldes 2007; 2012 because a different methodology was employed for each survey at different times. However the data collected is still of significant use for future research. As the same sample location along the reef system was used for both surveys and if researchers need base line data the same methodologies used in 1992, 2007 and 2012 can be adopted. The list of species presented in this research has the potential to be used as an excellent impact assessment tool in future investigations into physicochemical and anthropogenic effects of the reef system. Dr. Petrônio Alves Coelho was one of the most renowned taxonomists in species form the northeastern Brazilian coast and presents a very thorough identification of all species listed, allowing researchers to have confidence in any identifications published in the list of species. In addition almost all the survey specimens have been deposited in his collection at the Oceanographic Museum of the Federal University of Pernambuco, providing future researchers with a valuable voucher sample library which can be accessed at anytime for a species comparison. Unfortunately some of the biological material reported in the reviewed studies was also lost in transit from the field to the Oceanographic museum and due to the length of time between surveys some samples have received new taxonomic description.

4.1. Species of interest

The presence of Lysmata rathbunae Chace, 1970 in Porto de Galinhas, by Austregésilo-Filho(1992) and Coelho et al. (2002, 2006) needs to be confirmed as disregarded its presence on the Brazilian coast and reported the presence of two other species in its place, Lysmata ankeri Rhyne and Lin, 2006 and Lysmata bahia Rhyne and Lin, 2006. The reported by Rhyne and Lin in the 2006 study could however be Lysmata bahia, since it was reported to inhabit tidal-pools along the intertidal zone and displayed diurnal habit, in the same reef system sampled by Austregésilo-Filho(1992). Therefore it is 170 B.W. Giraldes et al. / Global Ecology and Conservation 3 (2015) 163–175

Fig. 5. Decapod abundance (%): Dominant species at Porto de Galinhas reef sampled in Subtidal and Intertidal zones. necessary to confirm the presence of Lysmata ankeri, Lysmata bahia, and Lysmata rathbunae in Pernambuco coastal reefs, because according to Rhyne and Lin(2006) none of these species occur in this state. Coelho et al.(2006) reports as uncertain the presence of L. rathbunae in Pernambuco. It is important that the presence of any of these Lysmata in the studied reef system is corroborated, as this will represent a newly recorded occurrence. The need of a species confirmation is also presented within Alpheus cf armillatus H. Milne Edwards, 1837 and Alpheus cf formosus Gibbes, 1850, as both species recorded belong to a complex of species (Soledade and Almeida, 2013). The snapping shrimp A. cf formosus in the study could be A. formosus because Anker et al.(2008) that described the complex of this species exclude the other species from Brazilian waters and the Pernambuco state. However specimens of Alpheus cf armillatus described in the Pernambuco region, according with Soledade and Almeida(2013) could be two different species, Alpheus carlae Anker, 2012 or Alpheus angulosus McClure, 2002. Caridea shrimp Brachycarpus holthuisi Fausto Filho, 1966 was recorded as a new occurrence for Pernambuco State, the species is endemic to Brazil but recorded only in the state of Ceará, in depths around 30–45 m without descriptions of color and habitat (Fausto Filho, 1966; Chace, 1972; Coelho et al., 2006). A reviewed study by Giraldes 2007;2012 discovered one example of Brachycarpus holthuisi (Fig. 6(A)–(F)) which was collected and identified during a SCUBA survey; and more individuals were observed and photographed in the reef caves. At the time it was misidentified as being B. biunguiculatus, however the work in this research confirmed the species as Brachycarpus holthuisi. Only three species of genus Brachycarpus exist in the world (De Grave et al., 2009) and only two occur in Brazil (Coelho et al., 2006) all with first two pereiopods with chela and the second pair is longer, smooth and more robust. The Brachycarpus recorded during this research present some features described only for B. holthuisi by Fausto Filho(1966) and Chace(1972) such as: the carpus of first cheliped being short and thin and almost as long as the chela (Fig. 6(F)); carpus of second pereiopod is longer and slender and about half longer than the merus, and slightly as long as palm of chela (Fig. 6(F)) telson is narrower and 1,5 longer than six abdominal segment. In addition the recorded B. holthuisi in this study present a uniform orange colored pattern on the whole body (Fig. 6(B) and (E)). Similarly Fausto Filho(1966) recorded uniform color pattern in preserved animals without reporting the color details. It should also be noted that B. biunguiculatus collected in this work even after being conserved in alcohol for a long time still presented color details on the body and in the dactyl of large cheliped (Fig. 6(G)). B. holthuisi, was recorded in this survey during night dives inside caves/grottos (Fig. 6(A)) around 4–8 m deep, and always inside small cavities in the substrate (Fig. 6(B) and (D)). It was noted during this research that B. holthuisi was a very retiring B.W. Giraldes et al. / Global Ecology and Conservation 3 (2015) 163–175 171

Fig. 6. Brachycarpus holthuisi Fausto Filho, 1966 (A)–(F), photographed at night inside the cave reef in studied area, being: (A) features of cave with one specimen localized inside; (B) the uniform color; (C) chelipeds details; (D) the telson and uropods details; (E) color pattern in the anterior body part and proportion details of walking pereiopods [WP] cheliped [Q] and third maxiliped [TM]; and (F) detailed drawing from first [small] and second [large] chelipeds extracted from picture E, highlighting the size of carpus compared with chelae. Brachycarpus biunguiculatus (Lucas, 1849) (G)–(J) being: (G) photographed in laboratory, highlighting the body proportion and the color details after long time conserved in alcohol 70%; (H) photographed at day in coastal reefs of Salvador—Bahia; (I) photographed at night in reef fringe on studied area; and (J) detailed drawing from first cheliped [small] and second cheliped [large] extracted from picture G, highlighting the size of carpus compared with chelae. Photographic credits: (H) Cláudio Luis Santos Sampaio; (A–G, I, J) Bruno Welter Giraldes. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.). species that immediately after being illuminated retreated back to its hiding-place, which made it extremely difficult to collect and photograph. This could explain why this shrimp was not recorded before 1966 and why only a few examples have been recorded in other states in northeastern Brazil and the Americas (Fausto Filho, 1966; Chace, 1972; Coelho et al., 2006). 172 B.W. Giraldes et al. / Global Ecology and Conservation 3 (2015) 163–175

The iconic species in this genus, B. biunguiculatus distinguished by its longer carpus in first minor cheliped; and shorter carpus in second large cheliped (Fausto Filho, 1966; Chace, 1972)(Fig. 6(J)) it also was photographed in the field during night dives. It was only found along the reef fringe near the water surface inside small cavities within the reef substrate (Fig. 6(I)). Voucher specimens were conserved in 70% alcohol and photographed in laboratory conditions (Fig. 6(G)). This report extends the geographical range of B. holthuisi to 700 km south of its present documented boundaries along the Brazilian coast. The study can also confirm the presence of B. holthuisi at approximately a depth 25 m higher than previously recorded. The research also presents unique photographs of the species in the field and the first description of its natural color pattern in the shallow water habitat. However the only specimen collected was lost during transportation from the field to the university and, there is no deposited specimen to confirm its presence and therefore this record can be considered as uncertain. The remainder of species sampled in Pernambuco state—Brazil (Coelho et al., 2002, 2006, 2007, 2008) reported here have specimens deposited at the oceanographic museum in Dr. Pertonio Alves Coelho collection at the Federal University of Pernambuco (MOUFPE).

4.2. Habitat and environmental divisions

This study was carried out in a reef bank along a large coastal reef ecosystem in the northeast coast of Brazil and the notable differences were recorded between decapod assemblages in relation to shore zones (intertidal and subtidal). The results suggest a natural habitat restriction for certain decapod assemblages in relation to shore zones along the whole coastal reef ecosystem (Dominguez et al., 1990; Maida and Ferreira, 1997; Leão et al., 2003). Some characteristics were common when targeting decapod assemblages in the intertidal zone or subtidal zones. Using the removal of substrate for a posteriori identification of the targeted species in intertidal samples (Table 1) were small and or very small decapods such as; Pitho lherminieri, Eurypanopeus abbreviatus, Hexapanopeus angustifrons, Acantholobulus schmitti, Panopeus hartii and Panopeus occidentalis (Melo, 1996); others have a definite association with epilithic algal matrix (EAM), that cover some lighted areas in the studied reefs; such as Cataleptodius floridanus, Macrocoeloma laevigatum, Microphrys bicornutus, Mithraculus forceps, Mithrax braziliensis, M. hemphilli, Acanthonyx dissimulatus, Epialtus bituberculatus and Pilumnus dasypodus (Melo, 1996; Melo and Veloso, 2005; Blanco et al., 2011). Others were have endobenthic behavior such as Upogebia affinis (Melo, 1999) and the Alpheoidea species such as A. armillatus, A. formosus, A. nuttingi, S. fritzmuelleri, S. longicarpus (Coelho et al., 2002; Almeida et al., 2008; Soledade and Almeida, 2013); or can be associated with the tidal-pool habitat of the intertidal zone such as; Paleomon northropi; Clibanarius antillensis, C. sclopettarius, Pachygrapsus transversus and Eriphia gonagra (Melo, 1996, 1999; Pralon and Negreiros-Fransozo, 2006; Coelho et al., 2002). In comparison the samples in the subtidal zone which were observed during nocturnal scuba diving could target large decapods that displayed nocturnal habits and are traded as ornamentals in aquarium stores or as commodities in fish mar- kets; species that inhabited cryptic ecotypes such as caves and grottoes in hard substrate; and possessed colors and features that enabled visual identification in situ. Decapods displaying these characteristics included the fished lobsters Panulirus argus, Panulirus echinatus and Panulirus laevicauda; the bycatch species Parribacus antarcticus, Palinurellus gundlachi, Dard- anus venosus, Petrochirus diogenes, Dromia erythropus, Mithrax hispidus, Mithrax braziliensis, Mithrax hemphilli, Mithraculus forceps, Menippe nodifrons, Carpilius corallinus, Calappa ocellata and Plagusia depressa; and ornamental decapods used in the aquarium trade such as; Brachycarpus biunguiculatus, Calcinus tibicen, Cinetorhynchus rigens, Dardanus venosus, Enoplometo- pus antillensis, Palinurellus gundlachi, Petrochirus diogenes, Platypodiella spectabilis, Stenopus hispidus, Mithraculus forceps and Stenorhynchus seticornis (Cervigón et al., 1992; Rocha et al., 1997; Melo, 1999; Calado et al., 2003; Gasparini et al., 2005; Corrêa et al., 2007; Freitas and Santos, 2007; Silva and Fonteles-Filho, 2011). Species with wide distribution inhabit the same intertidal zone in different biogeographic regions as in subtropical rocky reefs in southern and southwestern Brazil, and also are captured using the same methods described here such as Pachygrapsus transversus, Microphrys bicornutus, Mithraculus forceps, Eurypanopeus abbreviatus, Panopeus occidentalis, Pilumnus dasypodus, Petrolisthes galathinus, Clibanarius antillensis, C. sclopetarius Cuapetes americanus (as Periclimenes americanus) and Synalpheus fritzmuelleri(Masunari and Dubiaski-Silva, 1998; De Szechy et al., 2001; Turra and Denadai, 2001). In addition, following the functional equivalence, ecological equivalence or niche convergence theories (Hubbell, 2005, 2006), different species with the same genus but occurring in different biogeographic regions are reported as occupying the same habitat as species reported here: Pachycheles haigae Rodrigues da Costa, 1960, Pachycheles monilifer Dana, 1852, Megalobrachium roseum Rathbun, 1900, Acanthonyx petiverii H. Milne Edwards, 1834, Hexapanopeus paulensis Rathbun, 1930 and Epialtus brasiliensis Dana, 1852 reported to subtropical rocky reefs in intertidal zone at south and southern Brazil (Masunari and Dubiaski-Silva, 1998; De Szechy et al., 2001). The same is true for widely distributed species that inhabit cryptic habitats in the subtidal zones that have also been studied using scuba diving in temperate subtropical waters along rocky reefs in southern and southwestern Brazil, such as Mithraculus forceps, Mithrax hispidus, Pelia rotunda, Stenorhynchus seticornis, Menippe nodifrons, Calappa ocellata, Platypodiella spectabilis, Panulirus argus, Panulirus laevicauda, Enoplometopus antillensis and Stenopus hispidus. Also, species of the same genus that occur in cold subtropical waters were likewise reported using scuba diving as a sampling methodology in sub- tropical rocky reefs: Mithrax tortugae Rathbun, 1920, Calappa gallus (Herbst, 1803) and Dardanus insignis (de Saussure, 1858) (Gregati et al., 2006; Bouzon and Freire, 2007; Teschima et al., 2012). B.W. Giraldes et al. / Global Ecology and Conservation 3 (2015) 163–175 173

Therefore it is possible to find the same wide distribution of species inhabiting the same habitat and zone using the same sampling methodologies in different ecoregion (Spalding et al., 2007). According with each biogeographic ecoregion it is possible to find different species occupying the same habitat and niche and even within the same genus due to different environmental conditions and trophic pressures, (Hubbell, 2005, 2006) and certainly this mosaic of species distribution, biodiversity and biocenosis will oscillate according with several abiotic an biotic ranges. The present study revealed an interesting result with regards to the proportion of decapods in suborder and Infraorder because they present similar numbers of suborder with 1 Dendrobranchiata for each zone and 41 Pleocyemata in intertidal and 38 in subtidal zone; and the same number of species in some Infraorder as 21 Brachyura, 6 Anomura, and 1 Stenopodidea for each zone. Even with a similar proportion of Infraorder the composition of species was totally different highlighting the amazing specificity of habitat for decapod species. The differences in Infraorder composition in the intertidal zone in this study is accounted for by the high number of Caridea species present, the methodology involved the removal of substrate and this was reflected in the numbers of the Genus Alpheus and Synalpheus recorded during the work. These species are known for their high diversity and endoben- thic behavior (De Grave et al., 2009; Soledade and Almeida, 2013); the same is true of the Gebiidae an endobenthic group (Melo, 1999). In comparison only two Infraorder were recoded in the subtidal zone Astacidea and Achelata (Melo, 1999) and were encountered as a result of the use of scuba which allowed access to the caves and dark cavities in the subtidal reef struc- tures were these decapods frequent. These large lobsters with cryptic behavior will not appear along the intertidal zone or tidal-pools by day. The Brachyura followed by Caridea and Anomura represented the richest taxa in each sampled shore zone and for the studied reef system, similar to the findings described by Coelho et al.(2002) for the Pernambuco State in the northeast of Brazil (Coelho et al., 2006, 2007, 2008) and globally by De Grave et al.(2009). In addition, similar findings to those described in this research, show certain some taxa, such as; Alpheidae for Caridea and Majidae for Brachyura are prolific in numbers in Pernambuco State (Coelho et al., 2002, 2006, 2007, 2008) and in the world (De Grave et al., 2009). This proliferation has a long historical record for decapods in the ocean, with changes in speciation according ocean changes over a long period of time coupled with high adaptive values for groups with higher diversity; such as efficient body shape, productive strategies in obtaining food reproduction and defense (Távora et al., 2010). This is demonstrated within the brachyuran crabs that possess a great plasticity of shape, size and diet allowing them to live in several microhabitats (Melo, 1996), which explain their great diversity. This study highlights the importance of a habitat specific decapod checklist with descriptions of environmental and behavior relationships specific to each species. The absence or presence of decapod species within a specific zone can be an indicator of environmental disturbance from physicochemical or anthropic inputs. Mainly because the decapods represent one of the most important taxon in the marine ecosystem, being a key group in trophic relations within all marine trophic chains (Abele, 1974; Melo, 1996, 1999; Coelho et al., 2006, 2007, 2008; De Grave et al., 2009; Dubinsky and Stambler, 2011). Decapods are dominant within in a number of environmental niches such as; Cryptofauna that inhabit biogenic reefs (live deeply embedded within the interstitial reef spaces) and display symbiotic behavior with sessile organisms, providing important protection and defense to their hosts such as; algae, coral, zoanthid and echinoderms. They have a close trophic relationship with reef fish and provide a food source to many other species within the reef system (Randall, 1967; Wirtz et al., 2009; Stier et al., 2010; Stier and Leray, 2013). The quantitative result that displayed only a few dominant species, but high abundance and high frequency, for both methodologies, may be the natural decapod pattern for the investigated reef system. The high dominance displayed for only a few species is a typical climax characteristic of an old established ecosystems and this has been corroborated in previous studies carried out by Leão et al.(2003), who described the corals and hydrocorals that form the studied reefs in the northeast Brazil areas as archaic animals. The same author states that due to Amazon River plume, these local reefs have been preserved and remained isolated in Northeastern Brazil since the Pleistocene.

4.3. Scientific scuba diving as a research tool in decapod studies

Coelho et al.(2002) described 312 decapods for the Pernambuco state—Brazil, with a habitat division specific to each decapod assemblage which encompassed environments under a general heading such as; mangrove, marine soft bottom, coastal biogenic reefs (hard bottom), with a group of a few species occupying restricted zones and environments like the reef system described in this research. Therefore the 71 decapod species recorded during this intensive research of one reef struc- ture could be used as a representative template for the carcinofauna for costal reefs in the Pernambuco state. The current list of species also allows researchers to divide the species list further into habitat divisions, with 42 species listed as intertidal and 39 subtidal and with only 10 species occurring in both zones (Melo, 1996, 1999; Coelho et al., 2002; Wirtz et al., 2009). Almeida et al.(2008) completed a similar decapod checklist performed for a hard substrate habitat at a coastal island located close to the studied reefs. Differences of decapod composition between Almeida et al.(2008) and this study have been noted and can be attributed to a mangrove area close to were the samples were collected as the collected decapods displayed characteristics synonymous with estuarine areas. This study however employed scuba diving as a collection method and allowed the scientists access to more complex reef structures and therefore encounters with more ornamental and large decapods that live in cryptic habitats. The large similarities between the decapod assemblage in Almeida et al.(2008) and 174 B.W. Giraldes et al. / Global Ecology and Conservation 3 (2015) 163–175 the assemblage in this present study suggest that the species reported here represent the decapod assemblage in all coastal hard substrate environments in northeastern Brazil and can only oscillate influenced by external factors such as adjacent mangrove estuarine close to reef area. This study emphasis the value of adopting scuba diving as research tool when studying decapods, and agrees with Lang et al.(2013) that there has been a revolution in research and discoveries in marine sciences since the use of scuba diving within the last years. Without this tool it would have been virtually impossible to sample some of the species in this study such as: Janicea antiguensis, Brachycarpus holthuisi, Palinurellus gundlachi and Enoplometopus antillensis, and other decapods that display cryptic habits and are found in difficult to access areas of the reef. The use of scuba also allowed researchers describes new occurrences and distribution patterns for decapods in Brazilian waters (Mantelatto et al., 2004; Bouzon and Freire, 2007; Teschima et al., 2012; Alves et al., 2012; Giraldes et al., 2012a,b). The other great advantage of using scuba diving is it allows the scientist to study the decapod in-situ especially species like Panulirus argus, Panulirus echinatus and P. laevicauda, which are directly affected by the fishing market. The monitoring of these valuable species has the knock on effect of presenting the researcher an opportunity to study decapod species associated with the market dominant ones; Carpilius corallinus, Parribacus antarcticus, and Plagusia depressa usually found in local fishing markets and captured as bycatch species (Rocha et al., 1997); and some ornamental species traded and coveted by aquarium hobbyists such as Stenopus hispidus, Enoplometopus antillensis, Calcinus tibicen, Mithraculus forceps which in themselves command a high individual trade value Calado et al., 2003, Gasparini et al., 2005. In other words to study decapods comprehensively this research advises the use of scuba diving as it allows direct contact with the ecosystem and animals being studied. It offers a means of creating a visual census to compound information on the demands of a fishing industry targeting these crustaceans. Information obtained can be used to highlight public awareness of any detrimental impacts on stocks and can be used to inform authorities on the need to police stocks and manage and monitor accordingly. In conclusion, the use of scientific scuba diving to study decapods is an important addition to complement the traditional methodologies used when creating a decapod checklist and represents an important tool to study and monitoring the decapod assemblage in reef environments in general, especially in fragile coral reefs in protected marine areas.

Acknowledgments

Our main acknowledgment goes to the late renowned Dr. Petrônio Alves Coelho who enthusiastically initiated this study and was an active member of the research team, but unfortunately has not witnessed its conclusion. We also thank Cláudio Luis Santos Sampaio—Buia (Universidade Federal de Alagoas—UFAL), who provided additional color photograph used in Fig. 6(H).

References

Abele, L.G., 1974. Species diversity of decapod crustaceans in marine habitats. Ecology 55, 156–161. Almeida, A.O., Bezerra, L.E.A., Souza-Filho, J.F., Almeida, S.M., Albuquerque, D.L., Coelho, P.A., 2008. Decapod and stomatopod crustaceans from Santo Aleixo Island, state of Pernambuco, Brazil. Nauplius 16 (1), 23–41. Alves, D.F.R., Barros-Alves, S.P., Cobo, V.J., Lima, D.J.M., Fransozo, A., 2012. Checklist of the brachyuran crabs (Crustacea: ) in the rocky subtidal of Vitória Archipelago, southeast coast of Brazil. Check list 8 (5), 940–950. Anker, A., Hurt, C., Knowlton, N., 2008. Revision of the Alpheus formosus Gibbes, 1850 complex, with redescription of A. formosus and description of a new species from the tropical western Atlantic (Crustacea: Decapoda: Alpheidae). Zootaxa 1707, 1–22. Austregésilo-Filho, P.T., 1992. (Unpublished results) Crustáceos Estomatópodos e Decapodos dos recifes da praia de Porto de Galinhas (Sistemática e Ecologia). Monography, from Universidade Federal de Pernambuco—UFPE, Recife, p. 96. Barradas, J.I., Amaral, F.M.D., Hernández, M.I.M., Flores-Montes, M.J., Steiner, A.Q., 2010. Spatial distribution of benthic macroorganisms on reef flats at Porto de Galinhas Beach (northeastern Brazil), with special focus on corals and calcified hydroids. Biotemas 23 (2), 61–67. Blanco, C.G., Gusmão-Junior, J.B., Christofoletti, R.A., Costa, T.M., 2011. Hydrodynamism and its influence on the density of the decorator Microphrys bicornutus (Mithracidae) on intertidal rocky shores from a subtropical region. Mar. Biol. Res. 7 (7), 727–731. Bouzon, J.L., Freire, A.S., 2007. The Brachyura and Anomura fauna (Decapoda, Crustacea) in the Arvoredo Marine Biological Reserve on the southern Brazilian coast. Braz. J. Biol. 67, 321–325. Calado, R., Lin, J., Rhyne, A.L., Araújo, R., Narciso, L., 2003. Marine ornamental decapods—popular, pricey, and poorly studied. J. Crustac. Biol. 23, 963–973. Cervigón, F., Cipriani, R., Fischer, W., Garibaldi, L., Hendrickx, M., Lemus, A.J., Márquez, R., Poutiers, M., Roijaina, G., Rodriguez, B., 1992. Guia de Campo de las Especies Comerciales Marinas y de Aguas Salobras de la Costa Septentrional de Sur America. Organizacion de las Naciones Unidas para la Agricultura y la Alimentacion, Roma. Chace Jr., F.A., 1972. The shrimps of the Smithsonian–Bredin Caribbean Expeditions with a summary of the West Indian shallow-water species. Smithson. Contrib. Zool. 98, 1–179. Coelho, P.A., Almeida, A.O., Bezerra, L.E.A., 2008. Checklist of the marine and estuarine Brachyura (Crustacea: Decapoda) of northern and northeastern Brazil. Zootaxa 1956, 1–58. Coelho, P.A., Almeida, A.O., Bezerra, L.E.A., Souza Filho, J.F., 2007. An updated checklist of decapod crustaceans (infraorders Astacidea, Thalassinidea, Polychelida, Palinura, and Anomura) from the northern and northeastern Brazilian coast. Zootaxa 1519, 1–16. Coelho, P.A., Almeida, A.O., Souza Filho, J.F., Bezerra, L.E.A., Giraldes, B.W., 2006. Diversity and distribution of the marine and estuarine shrimps (Dendrobranchiata, Stenopodidea and Caridea) from North and Northeast Brazil. Zootaxa 1221, 41–62. Coelho, P.A., Ramos-Porto, M., 1995. Distribuição ecológica dos crustáceos decápodos marinhos do nordeste do Brasil. Trabalhos Oceanográficos da Universidade Federal de Pernambuco 23, 113–127. Coelho, P.A., Santos, M.A.C., Torres, M.F.A., Monteiro, B.R., Almeida, V.A.K., 2002. Reino animalia: filo (ou subfilo) crustácea no estado de pernambuco. In: Tabarelli, M., Silva, J.M.C. (Eds.), Diagnóstico da Biodiversidade de Pernambuco. Vol. 2. Secretaria de Ciência, tecnologia e Meio Ambiente, Editora Massangana, Recife, pp. 429–482. (Org.). Coelho-Filho, P.A., 2006. Checklist of the Decapods (Crustacea) from the outer continental shelf and seamounts from Northeast of Brazil—REVIZEE Program (NE III). Zootaxa 1184, 1–27. B.W. Giraldes et al. / Global Ecology and Conservation 3 (2015) 163–175 175

Corrêa, F.M., Giraldes, B.W., Silva, A.Z., 2007. Fauna acompanhante de crustáceos na pesca artesanal da lagosta pintada (Panulirus echinatus) em Tamandaré/PE. XII COLACMAR. Volume XII, April, Florianópolis, Brazil. Dajoz, R., 2005. Princípios de Ecologia, 7a ed. Artmed, p. 520. De Grave, S., Pentcheff, N.D., Ahyong, S.T., Chan, T.Y., Crandall, K.A., Dworschak, P.C., Felder, D.L., Feldmann, R.M., Fransen, C.H.J.M., Goulding, L.Y.D., Lemaitre, R., Low, M.E.Y., Martin, J.W., Ng, P.K.L., Schweitzer, C.E., Tan, S.H., Tshudy, D., Wetzer, R., 2009. A classification of living and fossil genera of decapod Crustaceans. Raffles Bull. Zool. Suppl. 21, 1–109. De Szechy, M.T.M., Veloso, V.G., De Paula, E.J., 2001. Brachyura (Decapoda, Crustacea) of phytobenthic communities of the sublittoral region of rocky shores of Rio de Janeiro and São Paulo, Brazil. Trop. Ecol. 42 (2), 231–242. Dominguez, J.M.L., Bittencourt, A.C.S.P., Leão, Z.M.A.N., Azevedo, A.E.G., 1990. Geologia do quaternário costeiro do estado de Pernambuco. Revista Brasileira de Geociências 20, 208–215. Dubinsky, Z., Stambler, N., 2011. Coral Reefs: An Ecosystem in Transition. Springer. Fausto Filho, J., 1966. Brachycarpus holthuisi, nova espécie de crustáceo do Brasil (Decapoda Palaemonidae). Arquivos da Estação Biologica Marinha da Universidade Federal do Ceará 6, 123–125. Freitas, A.E.T.S., Santos, M.C.F., 2007. Aspectos da biologia pesqueira do Aratu-da-Pedra Plagusia Depressa (Fabricius, 1775) (Crustacea, Brachyura, Plagusiidae) capturado em Tamandaré (Pernambuco–Brasil). Bol. Téc. Cient., CEPENE 15 (2), 39–46. Gasparini, J.L., Floeter, S.R., Ferreira, C.E.L., Sazima, I., 2005. Marine ornamental trade in Brazil. Biodivers. Conserv. 14, 2883–2899. Giraldes, B.W., 2007. (Unpublished results) Comunidade de Crustaáceos Decápodos Infralitorâneos dos Recifes da Praia de Porto de Galinhas (PE). Dissertação defendida em fevereiro de 2007 no Programa de Pós-Graduação em Oceanografia, da UFPE, p. 145. Giraldes, B.W., 2012. (Unpublished results) Decápodes infralitorâneos dos recifes costeiros de Pernambuco, nordeste do Brasil – uma abordagem com Censo Visual Subaquático noturno. Tese Defendida em Dezembro de 2012 no Programa de pós-Graduação em Oceanografia Biológica na UFPE, p. 174. Giraldes, B.W., Coelho Filho, P.A., Coelho, P.A., 2012a. Composition and spatial distribution of subtidal Decapoda on the ‘‘Reef Coast’’, northeastern Brazil, evaluated through a low-impact visual census technique. Nauplius 20 (1), 187–201. Giraldes, B.W., Coelho Filho, P.A., Coelho, P.A., Anker, A., 2012b. Confirmation of the presence of Janicea antiguensis (Chace, 1972) (Decapoda: Barbouriidae) in northeastern and eastern Brazil. Nauplius 20 (2), 171–178. Gregati, R.A., Pinheiro, A.P., Cobo, V.J., 2006. New records of Stenopus hispidus Olivier (Stenopodidae) and Enoplometopus antillensis Lütken (Enoplometopidae) in the Southeastern Brazilian coast. Pan-Amer. J. Aquat. Sci. 1 (1), 20–23. Hubbell, S.P., 2005. Neutral theory in community ecology and the hypothesis of functional equivalence. Funct. Ecol. 19 (1), 166–172. Hubbell, S.P., 2006. Neutral theory and the evolution of ecological equivalence. Ecology 87 (6), 1387–1398. Lang, M.A., Marinelli, R.L., Roberts, S.J., Taylor, P.R., 2013. Research and Discoveries: The Revolution of Science through Scuba. In: Smithsonian Contributions to the Marine Sciences, vol. 39. p. 258. Leão, Z.M.A.N., Kikuchi, R.K.P., Viviane, T., 2003. Corals and coral reefs of Brazil. In: Cortés, J. (Ed.), Latin American Coral Reefs. Elsevier, Amsterdam. Maida, M., Ferreira, B.P., 1997. Coral reefs of Brazil: an overview. In: Proc. 8th Int’l. Coral Reef Symporium, Panama, vol. 1, pp. 263–274. Manso, V.A.V., Corrêa, I.C., Guerra, N.C., 2003. Morfologia e sedimentologia da plataforma continental interna entre as praias de Porto de Galinhas e Campos— Litoral sul de Pernambuco, Brasil. Pesqui. Geociên. 30 (2), 17–25. Mantelatto, F.L.M., Faria, F.C.R., Biagi, R., Melo, G.A.S., 2004. Majoid crabs community (Crustacea: Decapoda) from infralittoral rocky/sandy bottom of Anchieta Island, Ubatuba, Brazil. Braz. Arch. Biol. Technol. 47, 273–279. Masunari, S., Dubiaski-Silva, J., 1998. Crustacea Decápodo da praia rochosa da Ilha do Farol, Matinhos, Paraná II. Distribuição espacial e densidade das populações. Rev. Bras. Zool. 15 (3), 643–664. Melo, G.A.S., 1996. Manual de Identificação dos Brachyura (caranguejos e siris) do litoral brasileiro. Museu de Zoologia. Universidade Estadual de São Paulo. FAPESP. Ed. Plêiade. Melo, G.A.S., 1999. Manual de Identificação dos Crustacea Decápodo do Litoral Brasileiro: Anomura, Thalassinidea, Palinuridea e Astacidea. Museu de Zoologia. Universidade Estadual de São Paulo. FAPESP. Ed. Plêiade. Melo, G.A.S., Veloso, V.G., 2005. The Brachyura (Crustacea, Decapoda) of the coast of the State of Paraíba Brazil, collected by project Algas. Rev. Bras. Zool. 22 (3), 796–805. Odum, E.P., Barrett, G.W., 2007. Fundamentos de Ecologia, 5a ed. Thomson Learning, São Paulo. Pralon, B.G.N., Negreiros-Fransozo, M.L., 2006. Population biology of Palaemon (Palaeander) northropi Rankin, 1898 (Crustacea, Decapoda, Palaemonidae) in a tropical South American estuary. Acta Limnologica Brasileira 18 (1), 77–87. Randall, J.E., 1967. Food Habits of Reef Fishes of the West Indies. In: Studies in Tropical Oceanography, vol. 5. University of Miami, pp. 655–847. Rhyne, A.L., Lin, J., 2006. A western Atlantic peppermint species complex: redescription of Lysmata wurdemanni (Gibbes), description of four new species and remarks on L. rathbunae Chace (Crustacea: Decapoda: Hippolytidae). Bull. Mar. Sci. 79, 165–204. Rocha, C.A., Franklin-Junior, W., Dantas, N.P., Farias, M.F., Oliveira, A.M.E., 1997. Fauna e flora acompanhantes da pesca da lagosta no nordeste do brasil. Bol. Téc. Cient. CEPENE 5 (1), 11–22. Silva, A.C., Fonteles-Filho, A.A., 2011. Avaliação do defeso aplicado à pesca da lagosta no nordeste do Brasil. v. 1. ed.. Editora Expressão Gráfica, Fortaleza. Soledade, G.O., Almeida, A.O., 2013. Snapping shrimps of the genus Alpheus Fabricius, 1798 from Brazil (Caridea: Alpheidae): updated checklist and key for identification. Nauplius 21 (1), 89–122. Spalding, M.D., Fox, H.E., Halpern, B.S., McManus, M.A., Molnar, J., Allen, G.R., Davidson, N., Jorge, Z.A., Lombana, A.L., Lourie, S.A., Martin, K.D., McManus, E., Molnar, J., Recchia, C.A., Robertson, J., 2007. Marine ecoregions of the world: a bioregionalization of coast and shelf areas. BioScience 57, 573–583. Stier, A.C., Leray, M., 2013. Predators alter community organization of coral reef cryptofauna and reduce abundance of coral mutualists. Coral Reefs http://dx.doi.org/10.1007/s00338-013-1077-2. Stier, A.C., McKeon, C.S., Osenberg, C.W., Shima, J.S., 2010. Guard crabs alleviate deleterious effects of vermetid snails on a branching coral. Coral Reefs 29, 1019–1022. Távora, V.A., Paixão, G.M.C., Silva, F.A., 2010. Considerações filogenéticas e biogeografia histórica dos malacostráceos (decápodes e isópodes) cenozóicos do Brasil. Rev. Bras. Geociên. 40 (1), 47–58. Teschima, M.M., Faria-Junior, E., Freire, A.S., 2012. New records of marine , crabs and lobsters (Crustacea) from Santa Catarina State, southern Brazil (27° 15′ S 48° 25′ W). Mar. Biodivers. Records 5 (1), 7. Turra, A., Denadai, M.R., 2001. Desiccation tolerance of four sympatric tropical intertidal hermit crabs (Decapoda, Anomura). Mar. Freshwater. Behav. Physiol. 34 (4), 227–238. Wirtz, P., Melo, G.S., de De Grave, S., 2009. Symbioses of decapod crustaceans along the coast of Espírito Santo, Brazil. Mar. Biodivers. Records 2 (e162), 1–9.